Cargando…

Environment-based object values learned by local network in the striatum tail

Basal ganglia contribute to object-value learning, which is critical for survival. The underlying neuronal mechanism is the association of each object with its rewarding outcome. However, object values may change in different environments and we then need to choose different objects accordingly. The...

Descripción completa

Detalles Bibliográficos
Autores principales: Kunimatsu, Jun, Yamamoto, Shinya, Maeda, Kazutaka, Hikosaka, Okihide
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7848585/
https://www.ncbi.nlm.nih.gov/pubmed/33468673
http://dx.doi.org/10.1073/pnas.2013623118
_version_ 1783645167161442304
author Kunimatsu, Jun
Yamamoto, Shinya
Maeda, Kazutaka
Hikosaka, Okihide
author_facet Kunimatsu, Jun
Yamamoto, Shinya
Maeda, Kazutaka
Hikosaka, Okihide
author_sort Kunimatsu, Jun
collection PubMed
description Basal ganglia contribute to object-value learning, which is critical for survival. The underlying neuronal mechanism is the association of each object with its rewarding outcome. However, object values may change in different environments and we then need to choose different objects accordingly. The mechanism of this environment-based value learning is unknown. To address this question, we created an environment-based value task in which the value of each object was reversed depending on the two scene-environments (X and Y). After experiencing this task repeatedly, the monkeys became able to switch the choice of object when the scene-environment changed unexpectedly. When we blocked the inhibitory input from fast-spiking interneurons (FSIs) to medium spiny projection neurons (MSNs) in the striatum tail by locally injecting IEM-1460, the monkeys became unable to learn scene-selective object values. We then studied the mechanism of the FSI-MSN connection. Before and during this learning, FSIs responded to the scenes selectively, but were insensitive to object values. In contrast, MSNs became able to discriminate the objects (i.e., stronger response to good objects), but this occurred clearly in one of the two scenes (X or Y). This was caused by the scene-selective inhibition by FSI. As a whole, MSNs were divided into two groups that were sensitive to object values in scene X or in scene Y. These data indicate that the local network of striatum tail controls the learning of object values that are selective to the scene-environment. This mechanism may support our flexible switching behavior in various environments.
format Online
Article
Text
id pubmed-7848585
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-78485852021-02-09 Environment-based object values learned by local network in the striatum tail Kunimatsu, Jun Yamamoto, Shinya Maeda, Kazutaka Hikosaka, Okihide Proc Natl Acad Sci U S A Biological Sciences Basal ganglia contribute to object-value learning, which is critical for survival. The underlying neuronal mechanism is the association of each object with its rewarding outcome. However, object values may change in different environments and we then need to choose different objects accordingly. The mechanism of this environment-based value learning is unknown. To address this question, we created an environment-based value task in which the value of each object was reversed depending on the two scene-environments (X and Y). After experiencing this task repeatedly, the monkeys became able to switch the choice of object when the scene-environment changed unexpectedly. When we blocked the inhibitory input from fast-spiking interneurons (FSIs) to medium spiny projection neurons (MSNs) in the striatum tail by locally injecting IEM-1460, the monkeys became unable to learn scene-selective object values. We then studied the mechanism of the FSI-MSN connection. Before and during this learning, FSIs responded to the scenes selectively, but were insensitive to object values. In contrast, MSNs became able to discriminate the objects (i.e., stronger response to good objects), but this occurred clearly in one of the two scenes (X or Y). This was caused by the scene-selective inhibition by FSI. As a whole, MSNs were divided into two groups that were sensitive to object values in scene X or in scene Y. These data indicate that the local network of striatum tail controls the learning of object values that are selective to the scene-environment. This mechanism may support our flexible switching behavior in various environments. National Academy of Sciences 2021-01-26 2021-01-18 /pmc/articles/PMC7848585/ /pubmed/33468673 http://dx.doi.org/10.1073/pnas.2013623118 Text en Copyright © 2021 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Kunimatsu, Jun
Yamamoto, Shinya
Maeda, Kazutaka
Hikosaka, Okihide
Environment-based object values learned by local network in the striatum tail
title Environment-based object values learned by local network in the striatum tail
title_full Environment-based object values learned by local network in the striatum tail
title_fullStr Environment-based object values learned by local network in the striatum tail
title_full_unstemmed Environment-based object values learned by local network in the striatum tail
title_short Environment-based object values learned by local network in the striatum tail
title_sort environment-based object values learned by local network in the striatum tail
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7848585/
https://www.ncbi.nlm.nih.gov/pubmed/33468673
http://dx.doi.org/10.1073/pnas.2013623118
work_keys_str_mv AT kunimatsujun environmentbasedobjectvalueslearnedbylocalnetworkinthestriatumtail
AT yamamotoshinya environmentbasedobjectvalueslearnedbylocalnetworkinthestriatumtail
AT maedakazutaka environmentbasedobjectvalueslearnedbylocalnetworkinthestriatumtail
AT hikosakaokihide environmentbasedobjectvalueslearnedbylocalnetworkinthestriatumtail